Spatial Orientation and the Vestibular System

Introduction Vestibular organs: The set of five organs—three semicircular canals and two otolith organs—located in each inner ear that sense head motion and head orientation with respect to gravity Also called the “vestibular labyrinth” or the “vestibular system” An often overlooked sense: The vestibular “sixth sense” Evolutionarily very old

Introduction The vestibular organs help us in many ways, for instance: Provide a sense of spatial orientation, consisting of Linear motion Angular motion Tilt Allow for the vestibulo-ocular reflex Stabilizes visual input by counter rotating the eyes to compensate for head movement

Figure 12.1 Demonstration of the vestibulo-ocular reflex SensationPerception3e-Fig-12-01-0.jpg

Introduction Problems with the vestibular system can lead to peculiar sensations: Spatial Disorientation: Any impairment of spatial orientation (i.e., our sense of linear motion, angular motion, or tilt) Dizziness: Nonspecific spatial disorientation Vertigo: A sensation of rotation or spinning Imbalance Blurred vision Illusory self-motion

Modalities and Qualities of Spatial Orientation Spatial orientation: A sense comprised of three interacting sensory modalities: Our senses of linear motion, angular motion, and tilt 1. Angular motion: Can be sensed when rotating head from side to side as if to say “no” 2. Linear motion: Sensed when accelerating or decelerating in a car 3. Tilt: Can be sensed when nodding head up and down as if to say “yes” Why considered different “modalities”? Sensing linear motion, angular motion, and tilt involves different receptors and/or different stimulation energy

Modalities and Qualities of Spatial Orientation Semicircular canals: The three toroidal tubes in the vestibular system that sense angular acceleration, a change in angular velocity Source of our sense of angular motion Otolith organs: The mechanical structures in the vestibular system that sense both linear acceleration and gravity Source of our sense of linear velocity and gravity

Modalities and Qualities of Spatial Orientation Coordinate system for classifying direction: x-axis: Points forward, in the direction the person is facing y-axis: Points laterally, out of the person’s left ear z-axis: Points vertically, out of the top of the head Axes are defined relative to the person, not relative to gravity

Figure 12.2 Movement of the head can be described in terms of a simple fixed coordinate system SensationPerception3e-Fig-12-02-0.jpg

Modalities and Qualities of Spatial Orientation Three directions for sense of rotation: Roll: Rotation around x-axis Pitch: Rotation around y-axis Yaw: Rotation around z-axis

Figure 12.3 Rotating bodies can move in three directions SensationPerception3e-Fig-12-03-0.jpg

Modalities and Qualities of Spatial Orientation Each spatial orientation modality can change in terms of its amplitude and direction Amplitude: The size (increase or decrease) of a head movement (e.g., angular velocity, linear acceleration, tilt) Direction: The line along which one faces or moves, with reference to the point or region toward which one is facing or moving

Modalities and Qualities of Spatial Orientation Linear motion Movements represented in terms of changes in the x-, y-, and z-axes Any arbitrary linear motion can be represented as a change along these three axes

Figure 12.4 Translating bodies can move in three directions SensationPerception3e-Fig-12-04-0.jpg

The Mammalian Vestibular System The vestibular organs do not respond to constant velocity They only respond to changes in velocity—acceleration Gravity and acceleration share a deep connection and can be considered equivalent

The Mammalian Vestibular System Hair cells: Support the stereocilia that transduce mechanical movement in the vestibular labyrinth into neural activity sent to the brain stem Mechanoreceptors: Sensory receptors that are responsive to mechanical stimulation (pressure, vibration, movement) Like the hair cells involved in hearing, hair cells act as the mechanoreceptors in each of the five vestibular organs Head motion causes hair cell stereocilia to deflect, causing a change in hair cell voltage and altering neurotransmitter release

Figure 12.6 The vestibular labyrinth is the nonhearing part of the inner ear SensationPerception3e-Fig-12-06-0.jpg

The Mammalian Vestibular System Hair cell responses In the absence of stimulation, hair cells release neurotransmitter at a constant rate When hair cell bundles bend, change in hair cell voltage is proportional to the amount of deflection Bending toward tallest stereocilia: Depolarization Bending away from tallest stereocilia: Hyperpolarization Hair cells increase firing to rotation in one direction and decrease firing to rotation in the opposite direction

Figure 12.7 Hair cell responses (Part 1) SensationPerception3e-Fig-12-07-1R.jpg

Figure 12.7 Hair cell responses (Part 2) SensationPerception3e-Fig-12-07-2R.jpg

Figure 12.7 Hair cell responses (Part 3) SensationPerception3e-Fig-12-07-3R.jpg

The Mammalian Vestibular System Semicircular canals Each one is about three-fourths of a toroid (donut) shape, measuring 15 mm long and 1.5 mm in diameter Canals are filled with a fluid called perilymph A second, smaller toroid is found inside the larger toroid, measuring 0.3 mm in diameter Formed by a membrane filled with fluid called endolymph Cross section of each canal swells substantially near where the canals join the vestibule: Ampulla

Figure 12.8 The semicircular canals (Part 1) SensationPerception3e-Fig-12-08-1R.jpg

Figure 12.8 The semicircular canals (Part 2) SensationPerception3e-Fig-12-08-2R.jpg

The Mammalian Vestibular System Semicircular canals (cont’d) Within the endolymph space of each ampulla is the crista Cristae: The specialized detectors of angular motion located in each semicircular canal in a swelling called the ampulla Each crista has about 7000 hair cells, associated supporting cells, and nerve fibers Cilia of hair cells project into jellylike cupula which forms an elastic dam extending to the opposite ampulla wall, with endolymph on both sides of dam When the head rotates, the inertia of the endolymph causes it to lag behind, leading to tiny deflections of the hair cells

The Mammalian Vestibular System Coding of direction in the semicircular canals Three semicircular canals in each ear Each canal is oriented in a different plane Each canal is maximally sensitive to rotations perpendicular to the canal plane

Figure 12.9 Each semicircular canal is maximally sensitive to rotations perpendicular to the canal plane SensationPerception3e-Fig-12-09-0.jpg

The Mammalian Vestibular System Push-pull symmetry Hair cells in opposite ears respond in a complementary fashion to each other When hair cells in the left ear depolarize, those in the analogous structure in the right ear hyperpolarize

Figure 12.10 The semicircular canals function in pairs that have a push-pull relationship (Part 1) SensationPerception3e-Fig-12-10-1R.jpg

Figure 12.10 The semicircular canals function in pairs that have a push-pull relationship (Part 2) SensationPerception3e-Fig-12-10-2R.jpg

The Mammalian Vestibular System Coding of amplitude in the semicircular canals In the absence of any rotation, many afferent neurons from the semicircular canals have a resting firing rate of about 100 spikes/s This firing rate is high relative to nerve fibers in other sensory systems High firing rate allows canal neurons to code amplitude by decreasing their firing rate, as well as increasing it Changes in firing rate are proportional to angular velocity of the head aligned with the canal the neuron is in

The Mammalian Vestibular System Semicircular canal dynamics Neural activity in semicircular canals is sensitive to changes in rotation velocity Constant rotation leads to decreased responding from the canal neurons after a few seconds

Figure 12.11 Response of a semicircular-canal neuron to constant-velocity rotation SensationPerception3e-Fig-12-11-0.jpg

The Mammalian Vestibular System Semicircular canal dynamics (cont’d) Canal afferent neurons are sensitive to back and forth rotations of the head, as well Greatest sensitivity to rotations at 1 Hz or less Faster rotations than 1 Hz would be dangerous Firing rate goes up and down as the head rotates back and forth The overall normalized amplitude of the canal neuron response scales with head rotation frequency

Figure 12.12 Sinusoidal motion trajectories (Part 1) SensationPerception3e-Fig-12-12-1R.jpg

Figure 12.12 Sinusoidal motion trajectories (Part 2) SensationPerception3e-Fig-12-12-2R.jpg

Figure 12.12 Sinusoidal motion trajectories (Part 3) SensationPerception3e-Fig-12-12-3R.jpg

The Mammalian Vestibular System Otolith organs sense acceleration and tilt Two otolith organs in each ear: Utricle: Contains about 30,000 hair cells Saccule: Contains about 16,000 hair cells Each organ contains a macula: A specialized detector of linear acceleration and gravity Each macula is roughly planar and sensitive primarily to shear forces Hair cells are encased in a gelatinous structure that contains calcium carbonate crystals called otoconia (“ear stones” in Greek)

Figure 12.13 The otolith organs (Part 1) SensationPerception3e-Fig-12-13-1R.jpg

Figure 12.13 The otolith organs (Part 2) SensationPerception3e-Fig-12-13-2R.jpg

The Mammalian Vestibular System Coding of amplitude in the otolith organs Larger accelerations (or larger gravitational shear forces) move the otolith organ’s otoconia more This leads to greater deflection of the hair cell bundles Change in receptor potential is proportional to magnitude of linear acceleration or gravitational shear

Figure 12.14 Activity of a vestibular neuron innervating the utricle (Part 1) SensationPerception3e-Fig-12-14-1R.jpg

Figure 12.14 Activity of a vestibular neuron innervating the utricle (Part 2) SensationPerception3e-Fig-12-14-2R.jpg

The Mammalian Vestibular System Coding of direction in the otolith organs Arises in part from the anatomical orientation of the organs Utricular macula: horizontal plane Sensitive to horizontal linear acceleration and gravity Saccular macula: vertical plane Sensitive to vertical linear acceleration and gravity

Spatial Orientation Perception Three experimental paradigms are typically used to investigate spatial orientation perception: Threshold estimation: What is the minimum motion needed to correctly perceive motion direction? Magnitude estimation: Participants report how much (e.g., how many degrees) they think they tilted, rotated, or translated Matching: Participants are tilted and then orient a line with the direction of gravity. This is done in a dark room with only the line visible to avoid any visual cues to orientation

Spatial Orientation Perception Rotation perception At first, constant rotation (in the dark) is perceived accurately Soon, however, subjects feel as if they are slowing down After 30 seconds, they no longer feel as if they are rotating Time course of habituation for perceived velocity is slower than time course of habituation for velocity neurons: “Velocity storage” When rotation stops, subjects feel as if they are rotating in the opposite direction

Figure 12.15 The angular velocity of a person at rest, with eyes closed, who was suddenly rotated at a constant speed for 50 seconds and then was abruptly returned to rest SensationPerception3e-Fig-12-15-0.jpg

Spatial Orientation Perception Yaw rotation thresholds Humans are so sensitive to yaw rotation that we can detect movements of less than 1 degree per second At this rate, it would take 6 minutes to turn completely around As yaw rotation frequency decreases, it takes faster movement to be detected

Figure 12.16 Mean velocity threshold as a function of frequency for seven subjects SensationPerception3e-Fig-12-16-0.jpg

Spatial Orientation Perception Translation perception When people are passively translated in the dark, they are able to use a joystick to reproduce the distance they traveled quite accurately Interestingly, they also reproduce the velocity of the passive-motion trajectory This implies that the brain remembers and replicates the velocity trajectory The otolith organs register acceleration, and our brains mathematically integrate the acceleration and turn it into the perception of linear velocity

Spatial Orientation Perception Tilt perception We are very accurate when perceiving tilt for angles between 0 degrees (upright) and 90 degrees (lying down) Illusion: If you roll tilt your head to the left or right while looking at a vertical streak of light, the light appears to tilt in the opposite direction

Figure 12.17 Subjects are generally pretty good at indicating how much they are tilted (Part 1) SensationPerception3e-Fig-12-17-1R.jpg

Figure 12.17 Subjects are generally pretty good at indicating how much they are tilted (Part 2) SensationPerception3e-Fig-12-17-2R.jpg

Figure 12.17 Subjects are generally pretty good at indicating how much they are tilted (Part 3) SensationPerception3e-Fig-12-17-3R.jpg

Sensory Integration Sensory integration: The process of combining different sensory signals Typically leads to more accurate information than can be obtained from individual senses alone

Sensory Integration Visual–vestibular integration Vection: An illusory sense of self motion produced when you are not, in fact, moving Example: The feeling of flying while watching an IMAX movie Example: Being stopped in your car at a light next to a semi. The semi begins to roll forward and you press on the brake because you feel as if you are rolling backwards

Sensory Integration Observers looking at a rotating display report rotational vection Subjects have the illusion of tilt but do not feel as if they turn upside-down Why don’t people feel as if they are turning upside down? The vestibular system’s sense of gravity stops the illusion Astronauts without gravity feel as if they are tumbling under these circumstances Thus, vestibular information is combined with visual information to yield a “consensus” about our sense of spatial orientation

Figure 12.18 Rotational vection SensationPerception3e-Fig-12-18-0.jpg

Reflexive Vestibular Responses Vestibulo-ocular reflexes (VORs): Counter-rotating the eyes to counteract head movements and maintain fixation on a target Angular VOR: The most well-studied VOR Example: When the head turns to the left, the eyeballs are rotated to the right to partially counteract this motion Torsional eye movements: When the head is rolled about the x-axis, the eyeballs can be rotated a few degrees in the opposite direction to compensate VORs are accomplished by six oculomotor muscles that rotate the eyeball

Figure 12.19 Contribution of the angular VOR to visual stability SensationPerception3e-Fig-12-19-0.jpg

Figure 12.20 Neural pathways for the angular-VOR three-neuron arc SensationPerception3e-Fig-12-20-0.jpg

Figure 12.21 VOR responses in the dark at three frequencies SensationPerception3e-Fig-12-21-0.jpg

Reflexive Vestibular Responses Vestibulo-autonomic responses Autonomic nervous system: The part of the nervous system innervating glands, heart, digestive system, etc., and responsible for regulation of many involuntary actions Motion sickness: Results when there is a disagreement between the motion and orientation signals provided by the semicircular canals, otolith organs, and vision Could be an evolutionary response to being poisoned Blood pressure is regulated by vestibulo-autonomic responses

Figure 12.23 Vestibular influences on blood pressure SensationPerception3e-Fig-12-23-0.jpg

Reflexive Vestibular Responses Vestibulo-spinal responses A whole family of reflexes that work together to keep us from falling over Without vestibulo-spinal responses, we would be unable to stand up in the dark Patients with vestibular loss actually over-compensate for body sway

Figure 12.24 Comparison of postural responses of subjects with normal vestibular function to responses of patients suffering severe bilateral vestibular loss SensationPerception3e-Fig-12-24-0.jpg

Figure 12.25 Neural pathways for vestibulo-spinal reflexes SensationPerception3e-Fig-12-25-0.jpg

Spatial Orientation Cortex We have a visual cortex and an auditory cortex; do we have a vestibular cortex? Not really Areas of cortex respond to vestibular input, but they tend to respond to visual input as well No need to have cortex for processing vestibular information in isolation if visual information is available also Vestibular information reaches the cortex via thalamo-cortical pathways Areas of cortex that receive projections from the vestibular system also project back to the vestibular nuclei Knowledge and expectations can influence perception of tilt and motion

Figure 12.26 Ascending vestibular pathways pass from the vestibular nuclei to the posterolateral thalamus on their way to the temporo-parieto-insular cortex SensationPerception3e-Fig-12-26-0.jpg

When the Vestibular System Goes Bad Since the vestibular system has such a widespread influence, what happens when it fails? Possible problems: Spatial disorientation Imbalance Distorted vision unless head is held perfectly still Motion sickness Cognitive problems

When the Vestibular System Goes Bad Mal de Debarquement Syndrome Swaying, rocking, or tilting perceptions felt after spending time on a boat or in the ocean Aftereffect of adapting to the rocking motion of the ocean “Getting your sea legs” Usually goes away after a few hours, but some people experience it continuously, causing problems

When the Vestibular System Goes Bad Ménière’s Syndrome Sudden experience of dizziness, imbalance, and spatial disorientation Can cause sudden falling down Can cause repeated vomiting from severe motion sickness The unpredictability of the attacks can be terrifying for those who suffer from it Possible treatments: medications, implanted devices, or sometimes removal of the vestibular apparatus itself!